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Abstract

Mammals have evolved circadian rhythms in internal biological processes and behaviors, such as locomotor activity (LA), to synchronize to the environmental conditions they experience. Photic entrainment of LA has been well established; however, non-photic entrainment, such as ambient temperature (T_a), has received much less attention. To address this dearth of knowledge, we exposed two subterranean endothermic-homeothermic African mole-rat species, the solitary Cape mole-rat (Georychus capensis [GC]) and social Mahali mole-rat (Cryptomys hottentotus mahali [CHM]), to varying T_a cycles in the absence of light. We showed that the LA rhythms of these two species entrain to T_a cycles and that the majority of LA occurred during the coolest 12-h period. LA confined to the coolest T_a periods may be the direct consequence of the poor heat dissipation abilities of African mole-rats brought about by physiological and ecological constraints. Recently, it has been hypothesized that T_a is only a strong zeitgeber for circadian rhythms in species whose thermoregulatory abilities are sensitive to changes in T_a (i.e., heterotherms and ectotherms), which previously has excluded endothermic-homeothermic mammals. However, this study demonstrates that T_a is a strong zeitgeber or entrainer for circadian rhythms of LA in subterranean endothermic-homeothermic mammals as a consequence of their sensitivity to changes in T_a brought about by their poor heat dissipation abilities. This study reinforces the intimate link between circadian rhythms and thermoregulation and conclusively, for the first time, provides evidence that T_a is a strong zeitgeber for endothermic-homeothermic mammals.

Keywords

ambient temperature mole-rat heat dissipation endothermic homeotherms entrainment

Mammals have evolved morphological, physiological, and behavioral traits in response to predictable environmental fluctuations (Piersma and Drent, 2003). One crucial trait is the ability to synchronize their internal biological processes and behaviors, such as locomotor activity (LA) patterns, to cyclic patterns of abiotic variables, for example, daily changes in light or ambient temperature (T_a) (Cloudsley-Thompson, 1961; Aschoff, 1966; Daan and Aschoff, 1975; Patel et al., 2014). The adaptive significance of innate circadian rhythmicity is thought to be related to the changes that arise in the environment of an organism, such as predator avoidance or food availability (so-called extrinsic advantages) (Boulos and Terman, 1980; O’Reilly et al., 1986; Boulos et al., 1989; Lima and Dill, 1990; Vaze and Sharma, 2013; Alagaili et al., 2020). It may also be through benefits derived from orchestrating internal biological processes such as maintaining metabolic activity and core body temperatures (T_b) (i.e., intrinsic advantage) (Boulos and Terman, 1980; O’Reilly et al., 1986; Boulos et al., 1989; Lima and Dill, 1990; Vaze and Sharma, 2013; Alagaili et al., 2020).

Light is arguably the most influential zeitgeber for the entrainment of circadian rhythms, and in particular, LA (DeCoursey and DeCoursey, 1964; Stephan and Zucker, 1972; Daan and Aschoff, 1975; Erkert et al., 1986; Goldman, 1999; Mahoney et al., 2001; Okamura et al., 2002; Verwey et al., 2013). It follows that the neuroanatomical pathways related to photic entrainment of the master circadian oscillator are well established (Reppert and Weaver, 2000; Shearman et al., 2000; Reppert and Weaver, 2001; Okamura et al., 2002; Mohawk et al., 2012). In contrast, non-photic entrainment of the circadian clock and the importance of circadian rhythms in conditions void of photic stimuli are far less understood.

In environments where reliable photic cues are absent, circadian rhythmicity has been demonstrated in several taxa, ranging from deep-sea or cave-dwelling invertebrates to subterranean rodents (reviewed by Abhilash et al. (2017)). Given the relatively stable environments of these dark habitats, the adaptive advantage of these circadian rhythms is primarily related to orchestrating internal physiological processes (Vaze and Sharma, 2013). However, data on the exact zeitgeber used for entrainment in species inhabiting environments where reliable photic cues are absent are limited, as most studies only report the presence or absence of a rhythm (Beale et al., 2016; Abhilash et al. 2017). Notwithstanding, changes in other non-photic cues have been proposed as potential zeitgebers in these stable dark environments, and one of importance to this study is T_a (Abhilash et al., 2017).

To date, only a limited number of studies have experimentally shown entrainment of LA patterns by daily T_a in mammals (Aschoff and Tokura, 1986; Rajaratnam and Redman, 1998; Pálková et al., 1999; Refinetti, 2010; Farsi et al., 2020). This existing body of research suggests that, in comparison with photic cues, T_a exhibits a varied effect on the circadian system depending on the species in question (Rajaratnam and Redman, 1998; Rensing and Ruoff, 2002; Refinetti, 2010). Recently, Farsi et al. (2020) hypothesized that the strength of T_a as a zeitgeber depends on the specific sensitivity of animals to changes in T_a. Indeed, for those species whose thermoregulatory states depend on T_a, such as heterothermic large desert mammals (Allali et al., 2013; Farsi et al., 2020) and ectotherms (Rensing and Ruoff, 2002), their circadian rhythms, like their T_b, are sensitive to changes in T_a and readily entrain to it. In contrast, for endothermic homeotherms, like many rodent species, a weak effect of T_a on the circadian system has been found (Rajaratnam and Redman, 1998; Rensing and Ruoff, 2002; Refinetti, 2010). The weak effect of T_a on the circadian rhythms of endothermic homeotherms has been hypothesized as the direct consequence of their constant T_b irrespective of the daily T_a cycle, resulting in these species being less sensitive to T_a changes (Rajaratnam and Redman, 1998; Rensing and Ruoff, 2002; Refinetti, 2010). However, these studies have been confined to mammals that are readily exposed to photic cues, and as a consequence, the evolutionary pressures behind this form of entrainment and its prevalence among mammals not exposed to photic cues are still unclear.

African mole-rats (Bathyergidae) are a subterranean family of rodents endemic to sub-Saharan Africa who rarely, if ever, venture to the surface (Bennett and Faulkes, 2000). Sociality within this family ranges from solitary to eusocial species (Bennett and Faulkes, 2000; Hart et al., 2021), and their thermoregulatory abilities range from endothermic homeothermy (Šumbera, 2019; Wallace et al., 2021) to heterothermy (Boyles et al., 2012; Oosthuizen et al., 2021) and even poikilothermy (Buffenstein and Yahav, 1991). The subterranean niche provides a relatively thermostable environment (Bennett et al., 1988; Šumbera et al., 2004; Holtze et al., 2018; Šumbera, 2019) as well as a shelter from above-ground predators and temperature extremes (Bennett and Faulkes, 2000; Finn et al., 2020), but the burrow systems have hypoxic and hypercapnic atmospheres with poor ventilation, high humidity, and limited access to light (Kennerly, 1964; Darden, 1972; Roper et al., 2001; Ivy et al., 2020; Logan et al., 2020). Although the burrow systems of African mole-rats are considered to possess a muted T_a range, a minor T_a range does exist (~10 °C) (Roper et al., 2001; Haupt et al., 2017). Furthermore, the LA of mole-rats under natural conditions has been suggested to be constrained by the risk of overheating during bouts of activity (Šklíba et al., 2014; Oosthuizen et al., 2021; Vejmělka et al., 2021), but there is no direct evidence to support this. The combination of subterranean existence, varied thermoregulatory abilities, and apparent sensitivity to overheating during activity make the members of the family Bathyergidae an ideal taxon to test the idea that entrainment to T_a is dependent on the sensitivity to temperature (i.e., thermoregulation strategy).

The LA patterns of African mole-rats have been extensively investigated and shown to entrain to photic stimuli, which suggests the possession of endogenous rhythms and a functional circadian system (Oosthuizen et al., 2003; Vasicek et al., 2005; Schöttner et al., 2006; De Vries et al., 2008; Streicher et al., 2011; Haupt et al., 2017; van Jaarsveld et al., 2019). Nevertheless, the degree of rhythmicity and ability to entrain varies within and between species (reviewed by Bennett (2009)). A recent study on the social endothermic-homeothermic Mahali mole-rat (Cryptomys hottentotus mahali [CHM]) suggested that both LA and T_b may be capable of synchronizing to T_a cycles; however, the experimental setup was unable to definitively prove this as the authors could not differentiate between masking and entrainment (van Jaarsveld et al., 2019).

We attempt to prove that T_a is a strong zeitgeber of circadian rhythms of LA in endothermic-homeothermic African mole-rats, given the lack of a reliable photic cue in the subterranean environment and the suggested sensitivity of LA to T_a, as a consequence of avoiding overheating while being active. To accomplish this, we used two species of African mole-rats, namely, the solitary Cape mole-rat (Georychus capensis [GC]) (Lovegrove and Papenfus, 1995; Oosthuizen et al., 2003) and social Mahali mole-rat (van Jaarsveld et al., 2019; Hart et al., 2020; Fagir et al., 2021). Both genera of Cryptomys (Boyles et al., 2012) and Georychus (Okrouhlík et al., 2021) have not been observed to exhibit heterothermy or poikilothermy, but are considered strict homeothermic endotherms.

Materials and Methods

Study Animals

Twelve CHM (82.6 ± 24.4 g, n = 12; male = 6, female = 6) and 12 GC (161.2 ± 43.7 g, n = 12; male = 5, female = 7) were used for this study. All animals were maintained and acclimated in captivity for longer than 1 year prior to the initiation of the experiments. All mole-rats were captured using modified Hickman traps (Hickman, 1979). GCs were caught during the austral summer in 2018 (January) in the Western Cape, South Africa (33°23′55.2″S, 18°25′06.4″E). CHM individuals were captured from the north-western most region of Gauteng, South Africa (25°39′48.0″S, 28°02′22.5″E), during the austral spring (September) 2018. Captured animals were transported back to the University of Pretoria Small Animal Physiological Research Facility (25°44′49.9″S, 28°15′31.7″E), where they were kept in a temperature constant room (26 °C) on a 12L:12D lighting regime. All animals were housed individually in plastic containers (83 × 44 × 37 cm) and maintained on an ad libitum diet of sweet potatoes, which were replaced on a daily basis to avoid any increases in activity levels associated with foraging (Vasicek et al., 2005). To avoid entrainment to a fixed feeding time, the animals were fed at varying times of the day and night (Golombek and Rosenstein, 2010). All animals were provided with wood shavings and paper towels for nesting material. A study conducted by Bennett and Jarvis (1995) showed that sweet potatoes provide mole-rats with more than 90% of their water and nutritional needs.

Between experimental cycles, plastic containers were cleaned by replacing the wood shavings and the paper toweling. Rooms were fitted with double doors to ensure the integrity of the light and temperature cycles inside the room. A dim red light was used during feeding and cleaning times if this occurred during the dark phase as well as during the constant dark (DD) conditions (light intensity <1 lux).

Experimental Protocol

The experimental protocol was conducted in the climate-controlled rooms of the Small Animal Physiological Research Facility at the University of Pretoria. We are able to regulate the temperature and lighting in the climate rooms in this facility to duplicate sinusoidal patterns in Ta and light cycles. Animals were subjected to a habituation period of 14 days (Cycle 1), followed by three experimental cycles ranging from 21 to 42 days (see Table 1). During Cycle 1, animals were subjected to 10L:14D and constant T_a of 25 °C, and lights went on at 0700 h and off at 1700 h (Figure 1a). To investigate whether the circadian rhythms of LA of CHM and GC are capable of entraining to T_a cycles in the absence of light, we subjected animals to complete darkness (DD) and a simulated T_a cycle, Cycle 2, mimicking the natural range of temperatures experienced by these animals in their burrow systems (18-28 °C) (Roper et al., 2001; Haupt et al., 2017) (Figure 1b). Cycle 2 was followed by constant conditions (DD, T_a = 25 °C), Cycle 3, to differentiate whether any observed rhythms were due to masking or entrainment (Figure 1c). Thereafter, we moved the T_a cycle forward 6 h—Cycle 4—to test whether rhythms would re-entrain to the temperature stimulus (Figure 1d). All procedures involving live animals and sample collection described in this article were conducted in accordance with the appropriate national and provincial guidelines, permits, and regulations. The study was approved by the animal ethics committee of the University of Pretoria, and the ethics certificate approval number is EC038-18.

Table 1.

Number of days spent in each experimental cycle for 12 Mahali mole-rats (Cryptomys hottentotus mahali [CHM]) and 12 Cape mole-rats (Georychus capensis [GC]).

Species	Number of days
Species	Habituation/Cycle 1	Cycle 2	Cycle 3	Cycle 4
CHM	14	31	21	40
GC	14	36	42	33

Figure 1.

Experimental conditions during the (a) habituation period/Cycle 1, (b) Cycle 2, (c) Cycle 3, and (d) Cycle 4. Solid lines indicate the T_a profile, whereas gray and white bars indicate the absence or presence of light, respectively.

LA Recording

Infrared motion detector (Quest PIR internal passive infrared detector; Elite Security Products [ESP], Electronic Lines, UK) was used to record LA for each mole-rat. The motion detectors were positioned over the containers such that all LA on the floor space of the container was detected. Consequently, the recorded LA readings were summed per minute and relayed to a computer using the program Vitalview (Vital ViewTM, Minimitter Co., Inc., Sunriver, OR, USA; www.minimitter.com).

Statistical Analysis

Actograms and tau (τ) of LA were calculated using RythmicAlly in R (R Development Core Team 2018; Abhilash and Sheeba, 2019). To assess whether body mass and sex influenced proportion, we conducted generalized linear mixed-effects models on hourly proportions data for Cycles 2 and 4, for each species, separately, using the lme4 package (Bates et al., 2015). Each model contained cycle, the body mass and sex of the mole-rat, and called on the binomial distribution (Bates et al., 2015). Each model included individual ID as a random factor to account for pseudoreplication. We refrained from commenting on total counts of activity as biotic and abiotic factors readily influence this. Reported values are presented as the percentage of activity within a cycle for each hour of the day (Equation 1):

Hourly activity (%) = \frac{\sum_{i = 1}^{24} counts}{\sum counts} \times 100

(1)

Results

During Cycle 1, both species confined the majority of their activity to the dark phase of the LD cycle (Figure 2). CHM and GC displayed 86% and 79% of activity during the dark phase (1700 h to 0700 h).

Figure 2.

Representative actograms of locomotor activity for (a) Mahali mole-rat (Cryptomys hottentotus mahali) and (b) Cape mole-rat (Georychus capensis) individuals. Actograms are double-plotted with time on the x-axis. During the habituation period/Cycle 1, air temperature (T_a) was 25 °C, and the lights went on at 0700 h and off at 1700 h. Cycle 2 consisted of constant darkness (DD) and a natural temperature ramp (18-28 °C), with a nadir at 0300 h. During Cycle 3, animals were subject to DD and 25 °C. Cycle 4 consisted of DD and a 6-h shift from Cycle 2 in the natural temperature ramp, with a nadir at 0900 h. Color bar indicates temperature gradient, with dark red representing the hottest period (28 °C) and dark blue representing the coolest period (18 °C).

When subjected to DD conditions in the presence of a natural T_a ramp (Cycle 2), LA became confined to the coolest hours of the cycle (18-23 °C) in both species (Figures 2 and 3). CHM displayed 80% of activity in the coolest 12 h of the cycle, and GC displayed 68% of their activity during the same period (Figure 3).

Figure 3.

Percentage (%) of daily locomotor activity expressed per hour for (a) 12 Mahali mole-rats (Cryptomys hottentotus mahali) and (b) 12 Cape mole-rats (Georychus capensis). Cycle 2 (purple) consisted of constant darkness (DD) and a natural temperature ramp, with a nadir at 0300 h. Cycle 4 (green) consisted of DD and a 6-h shift in the natural temperature ramp, with a nadir at 0900 h. Color bar indicates temperature gradient, with dark red representing the hottest period (28 °C) and dark blue representing the coolest period (18 °C).

Eight of the 12 CHM displayed a free-running period under constant DD conditions, with an average τ of 23.9 ± 0.37 h (Cycle 3; Figure 2). Ten of the 12 GC individuals displayed a free-running period under constant conditions, with an average τ of 24.12 ± 0.39 h (Cycle 3; Figure 2).

When released from constant conditions and subjected to a T_a cycle advanced by 6 h, both CHM and GC displayed a phase advance and re-entrainment of LA to the coolest hours of the cycle (Cycle 4; Figures 2 and 3). The proportion of activity expressed during the 12 coolest hours (18-23 °C) was 75% in CHM, whereas GC displayed 75% of their activity in the same period (Figure 3).

Experimental cycle had a significant effect on hourly proportions of LA for both species (CHM: z = 4.231, p < .001; GC: z = −6.889, p < .001). For CHM, hourly proportions were higher in Cycle 4 compared to Cycle 2, while the reverse was observed for GC. No effect of sex (CHM: z = 0.614, p = .539; GC: z = 1.795, P = .073) or body mass (CHM: z = −0.713, p = .476; GC: z = −0.004, p = .997) was reported for either species.

Discussion

In this study, under DD conditions in the presence of a 24-h T_a cycle, both species displayed a preference for increased LA during the cooler period (18-23 °C) of the 24 h cycle—rather than the warmer period (23-28 °C). Therefore, it is evident that LA is able to synchronize, through entrainment, to T_a cycles, a result that is in agreement with previous studies on mammals (Rajaratnam and Redman, 1998; Rensing and Ruoff, 2002; Refinetti, 2010, van Jaarsveld et al., 2019). However, it is essential to distinguish between entrainment and masking effects of T_a on LA (Golombek and Rosenstein, 2010; Bittman, 2021). The data presented here present two lines of evidence that oppose the notion that LA rhythm is synchronized to T_a through masking. First, when animals were released into constant conditions (i.e. Cycle 3), the free-running rhythms begin from the same place as the prior entrained rhythm (i.e. Cycle 2) and display drift (Daan and Aschoff, 2001; Refinetti, 2015). In addition, a 6-h phase advance in the daily T_a cycle, from free-running conditions, resulted in a progressive shift in LA patterns (~6 h), with peak activity again present in the cooler periods of the T_a cycle (Daan and Aschoff, 2001; Refinetti, 2015). Together, LA rhythm persistence under free-running conditions and progressive phase-matching of free-running rhythms to 6-h advance in T_a cycle favor the notion of entrainment of LA by T_a in the two species of African mole-rat. To the best of our knowledge, this is the first evidence of temperature entrainment in subterranean rodents.

Both species were most active at T_a well below their thermoneutral zones, subsequently increasing the energetic costs of locomotion. The coolest 12 h of the T_a cycles were between 18 and 23 °C, while the thermoneutral zone for CHM and GC lies between 27 and 32 °C (Wallace et al., 2021) and 26 and 34 °C (Lovegrove, 1987), respectively. CHM and GC may tolerate the energetic demands of increased energetics under their respective thermoneutral zone for two possible reasons. First, by using T_a as a zeitgeber and confining LA to the cooler periods, GC and CHM may be avoiding exercise-induced hyperthermia associated with the metabolic heat gains from burrowing (McNab, 1974; Speakman and Król, 2010). This condition may be further exacerbated by the poor evaporative cooling capabilities present in these two species of burrowing mammals (Luna et al., 2020; Wallace et al., 2021). Consequently, these mole-rats are unable to physiologically dissipate heat efficiently, further increasing the risk of exercise-induced hyperthermia. This is congruent with field studies that found mole-rats confine activity to the cooler periods (Streicher et al., 2011; Šklíba et al., 2014; Vejmělka et al., 2021). Second, foraging underground is energetically more expensive than above-ground living (Vleck, 1979). Geophytes, which provide the only source of food and water, are unevenly dispersed in their habitat, resulting in even more significant energetic expenditure (digging) to locate their food sources (Bennett and Faulkes, 2000). Traditional resource-based ecological and evolutionary theories assume that energetic constraints are directly affected as a consequence of resource availability (Luna et al., 2020). However, according to the Heat Dissipation Limit theory, the energetics of an endotherm could possibly increase through enhanced heat dissipation capacity (Speakman and Król, 2010). Thus, increased activity during the cooler periods may potentially allow for increased energetic output during LA.

In the past, homeothermic mammals have been recorded to show weak entrainment to T_a (Rajaratnam and Redman, 1998; Rensing and Ruoff, 2002; Refinetti, 2010); it is permissible to predict that GC and CHM would also show weak responses to T_a. However, when considering the limited heat dissipation ability brought about by physiological and ecological constraints, it is clear that these species are indeed sensitive to T_a changes, resulting in their strong LA entrainment by T_a. Moreover, the lack of a reliable photic cue makes T_a a more reliable “time-keeping” variable in the subterranean environment to which GC and CHM entrain.

In conclusion, these results favor the hypothesis put forward by Farsi et al. (2020), namely that the strength of T_a as a zeitgeber depends on the sensitivity (often linked to the thermoregulatory abilities of the species) of a species to daily T_a changes. In addition, we show that T_a is a reliable cue that social and solitary African mole-rats are capable of perceiving and subsequently use to entrain LA rhythms. Finally, the nocturnal LA patterns in many African mole-rat species could possibly be a consequence of the requirement to be active during the cooler periods of the day. The African mole-rats may be the ideal model family, with a diverse range of thermoregulatory abilities, to unravel the relationship between thermoregulation, circadian rhythmicity, and the subsequent molecular machinery behind this relationship, which are currently unknown.

Footnotes

Acknowledgements

We are grateful to the Gauteng Department of Nature Conservation and the Western Cape Department of Nature Conservation for permits to collect CHMs (CPF6-0127) and GCs (AAA041-00169-0056), respectively. We thank the respective landowners Mr. John Duckett (Western Cape) and the Kemp family (Gauteng) for allowing us to trap mole-rats on their farms. We thank the two anonymous reviewers for their insightful comments that improved the quality of this manuscript. This study was funded by SARCHI Chair of Mammal Behavioural Ecology and Physiology to N.C.B. (grant no. 64756).

Author Contributions

D.W.H., B.v.J., M.K.O., and N.C.B. conceptualized the project. D.W.H. and K.L.G. collected data and performed animal maintenance. B.v.J. and K.G.L. analyzed the data. All authors contributed toward the writing of the manuscript and agreed to be held accountable for the content therein.

Conflict of Interest Statement

The author(s) have no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

ORCID iDs

Daniel W. Hart

Maria K. Oosthuizen

Data Accessibility

The data and code are archived on GitHub ().

References

Abhilash

Sheeba

(2019) RhythmicAlly: your r and shiny–based open-source ally for the analysis of biological rhythms. J Biol Rhythms 34:551-561.

Abhilash

Shindey

Sharma

(2017) To be or not to be rhythmic? A review of studies on organisms inhabiting constant environments. Biol Rhythm Res 48:677-691.

Alagaili

Bennett

Amor

Hart

(2020) The locomotory activity patterns of the arid-dwelling desert hedgehog, Paraechinus aethiopicus, from Saudi Arabia. J Arid Environ 177:104141.

Allali

El Achaâban

Bothorel

Piro

Bouâouda

Allouchi

El Ouassat

Malan

Pévet

(2013) Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Integr Comp Physiol 304:R1044-R1052.

Aschoff

(1966) Circadian activity pattern with two peaks. Ecology 47:657-662.

Aschoff

Tokura

(1986) Circadian activity rhythms in squirrel monkeys: entrainment by temperature cycles. J Biol Rhythms 1:91-99.

Bates

Maechler

Bolker

Walker

(2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1-48.

Beale

Whitmore

Moran

(2016) Life in a dark biosphere: a review of circadian physiology in ‘arrhythmic’ environments. J Comp Physiol B 186:947-968.

Bennett

(2009) African mole-rats (family bathyergidae): models for studies in animal physiology. African Zool 44:263-270.

10.

Bennett

Faulkes

(2000) African mole-rats: ecology and eusociality. Cambridge (UK): Cambridge University Press.

11.

Bennett

Jarvis

JUM

(1995) Coefficients of digestibility and nutritional values of geophytes and tubers eaten by southern African mole-rats (Rodentia: Bathyergidae). J Zool 236:189-198.

12.

Bennett

Jarvis

JUM

Davies

(1988) Daily and seasonal temperatures in the burrows of African rodent moles. South African J Zool 23:189-195.

13.

Bittman

(2021) Entrainment is NOT synchronization: an important distinction and its implications. J Biol Rhythms 36:196-199.

14.

Boulos

Terman

(1980) Food availability and daily biological rhythms. Neurosci Biobehav Rev 4:119-131.

15.

Boulos

Frim

Dewey

Moore-Ede

(1989) Effects of restricted feeding schedules on circadian organisation in squirrel monkeys. Physiol Behav 45:507-515.

16.

Boyles

Verburgt

Mckechnie

Bennett

(2012) Heterothermy in two mole-rat species subjected to interacting thermoregulatory challenges. J Exp Zool Part A Ecol Genet Physiol 317A:73-82.

17.

Buffenstein

Yahav

(1991) Is the naked mole-rat Hererocephalus glaber an endothermic yet poikilothermic mammal? J Therm Biol 16:227-232.

18.

Cloudsley-Thompson

(1961) Rhythmic activity in animal physiology and behaviour. New York: Academic Press.

19.

Daan

Aschoff

(1975) Circadian rhythms of locomotor activity in captive birds and mammals: their variations with season and latitude. Oecologia 18:269-316.

20.

Daan

Aschoff

(2001) The entrainment of circadian systems. In: Takahashi

Turek

Moore

, editors, Circadian clocks. Boston (MA): Springer. p. 7-43.

21.

Darden

(1972) Respiratory adaptations of a fossorial mammal, the pocket gopher (Thomomys bottae). J Comp Physiol 78:121-137.

22.

De Vries

Oosthuizen

Sichilima

Bennett

(2008) Circadian rhythms of locomotor activity in Ansell’s mole-rat: are mole-rat’s clocks ticking? J Zool 276:343-349.

23.

DeCoursey

(1964) Adaptive aspects of activity rhythms in bats. Biol Bull 126:14-27.

24.

Erkert

Nagel

Stephani

(1986) Light and social effects on the free-running circadian activity rhythm in common marmosets (Callithrix jacchus; Primates): social masking, pseudo-splitting, and relative coordination. Behav Ecol Sociobiol 18:443-452.

25.

Fagir

Bennett

Ueckermann

Howard

Hart

(2021) Ectoparasitic community of the Mahali mole-rat, Cryptomys hottentotus mahali: potential host for vectors of medical importance in South Africa. Parasites Vectors 14:24.

26.

Farsi

Harti

Achaâban

Piro

Raverot

Bothorel

Ouassat

Challet

Pévet

El Allali

(2020) Melatonin rhythm and other outputs of the master circadian clock in the desert goat (Capra hircus) are entrained by daily cycles of ambient temperature. J Pineal Res 68:e12634.

27.

Finn

Voigt

van Jaarsveld

Hart

Jorna

(2020) PSEUDASPIS CANA (mole snake). Herpetol Rev 51:626-627.

28.

Goldman

(1999) The circadian timing system and reproduction in mammals. Steroids 64:679-685.

29.

Golombek

Rosenstein

(2010) Physiology of circadian entrainment. Physiol Rev 90:1063-1102.

30.

Hart

Medger

van Jaarsveld

Bennett

(2020) Is the Mahali mole-rat (Cryptomys hottentotus mahali) a spontaneous or induced ovulator? Can J Zool 98:299-305.

31.

Hart

Medger

van Jaarsveld

Bennett

(2021) Filling in the holes: the reproductive biology of the understudied Mahali mole-rat (Cryptomys hottentotus mahali). Can J Zool. doi:10.1139/cjz-2020-0158

32.

Haupt

Bennett

Oosthuizen

(2017) Locomotor activity and body temperature patterns over a temperature gradient in the Highveld mole-rat (Cryptomys hottentotus pretoriae). PLoS ONE 12:e0169644.

33.

Hickman

(1979) A live-trap and trapping technique for fossorial mammals. South African J Zool 14:9-12.

34.

Holtze

Braude

Lemma

Koch

Morhart

Szafranski

Platzer

Alemayehu

Goeritz

Hildebrandt

(2018) The microenvironment of naked mole-rat burrows in East Africa. Afr J Ecol 56:279-289.

35.

Ivy

Sprenger

Bennett

van Jaarsveld

Hart

Kirby

Yaghoubi

Storey

Milsom

Pamenter

(2020) The hypoxia tolerance of eight related African mole-rat species rivals that of naked mole-rats, despite divergent ventilatory and metabolic strategies in severe hypoxia. Acta Physiol 228:e13436.

36.

Kennerly

(1964) Microenvironmental conditions of pocket gopher burrow. Texas J Sci 16:395-441.

37.

Lima

Dill

(1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619-640.

38.

Logan

Szereszewski

Bennett

Hart

van Jaarsveld

Pamenter

Storey

(2020) The brains of six African mole-rat species show divergent responses to hypoxia. J Exp Biol 223:jeb215905.

39.

Lovegrove

(1987) Thermoregulation in the subterranean rodent Georychus capensis (Rodentia: Bathyergidae). Physiol Zool 60:174-180.

40.

Lovegrove

Papenfus

(1995) Circadian activity rhythms in the solitary Cape mole-rat (Georychus capensis: Bathyergidae) with some evidence of splitting. Physiol Behav 58:679-685.

41.

Luna

Šumbera

Okrouhlík

Mladěnková

Antenucci

(2020) Evaporative water loss in seven species of fossorial rodents: does effect of degree of fossoriality and sociality exist? J Therm Biol 89:102564.

42.

McNab

(1974) The energetics of endotherms. Ohio J Sci 74:370-380.

43.

Mahoney

Bult

Smale

(2001) Phase response curve and light-induced fos expression in the suprachiasmatic nucleus and adjacent hypothalamus of Arvicanthis niloticus. J Biol Rhythms 16:149-162.

44.

Mohawk

Green

Takahashi

(2012) Central and peripheral circadian clocks in mammals. Annu Rev Neurosci 35:445-462.

45.

Okamura

Yamaguchi

Yagita

(2002) Molecular machinery of the circadian clock in mammals. Cell Tissue Res 309:47-56.

46.

Okrouhlík

Šumbera

Gardner

Schoemann

Lövy

Bennett

(2021) Are southern African solitary mole-rats homeothermic or heterothermic under natural field conditions? J Therm Biol 95:102810.

47.

Oosthuizen

Cooper

Bennett

(2003) Circadian rhythms of locomotor activity in solitary and social species of African mole-rats (family: bathyergidae). J Biol Rhythms 18:481-490.

48.

Oosthuizen

Robb

Harrison

Froneman

Joubert

Bennett

(2021) Flexibility in body temperature rhythms of free-living natal mole-rats (Cryptomys hottentotus natalensis). J Therm Biol 99:102973.

49.

O’Reilly

Armstrong

Coleman

(1986) Restricted feeding and circadian activity rhythms of a predatory marsupial, Dasyuroides byrnei. Physiol Behav 38:471-476.

50.

Pálková

Sigmund

Erkert

(1999) Effect of ambient temperature on the circadian activity rhythm in common marmosets, Callithrix j. jacchus (primates). Chronobiol Int 16:149-161.

51.

Patel

Eckel-Mahan

Sassone-Corsi

Baldi

(2014) How pervasive are circadian oscillations? Trends Cell Biol 24:329-331.

52.

Piersma

Drent

(2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228-233.

53.

R Development Core Team (2018) R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.

54.

Rajaratnam

SMW

Redman

(1998) Entrainment of activity rhythms to temperature cycles in diurnal palm squirrels. Physiol Behav 63:271-277.

55.

Refinetti

(2010) Entrainment of circadian rhythm by ambient temperature cycles in mice. J Biol Rhythms 25:247-256.

56.

Refinetti

(2015) Comparison of light, food, and temperature as environmental synchronizers of the circadian rhythm of activity in mice. J Physiol Sci 65:359-366.

57.

Rensing

Ruoff

(2002) Temperature effect on entrainment, phase shifting, and amplitude of circadian clocks and its molecular bases. Chronobiol Int 19:807-864.

58.

Reppert

Weaver

(2000) Comparing clockworks: mouse versus fly. J Biol Rhythms 15:357-364.

59.

Reppert

Weaver

(2001) Molecular analysis of mammalian circadian rhythms. Annu Rev Physiol 63:647-676.

60.

Roper

Bennett

Conradt

Molteno

(2001) Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. J Zool 254:101-107.

61.

Schöttner

Oosthuizen

Broekman

Bennett

(2006) Circadian rhythms of locomotor activity in the Lesotho mole-rat, Cryptomys hottentotus subspecies from Sani Pass, South Africa. Physiol Behav 89:205-212.

62.

Shearman

Sriram

Weaver

Maywood

Chaves

Zheng

Kume

Lee

Hastings

Reppert

(2000) Interacting molecular loops in the mammalian circadian clock. Science 288:1013-1019.

63.

Šklíba

Lövy

Hrouzková

Kott

Okrouhlík

Šumbera

(2014) Social and environmental influences on daily activity pattern in free-Living subterranean rodents: the case of a eusocial bathyergid. J Biol Rhythms 29:203-214.

64.

Speakman

Król

(2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726-746.

65.

Stephan

Zucker

(1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci 69:1583-1586.

66.

Streicher

Boyles

Oosthuizen

Bennett

(2011) Body temperature patterns and rhythmicity in free-ranging subterranean Damaraland mole-rats, Fukomys damarensis. PLoS ONE 10:e26346.

67.

Šumbera

(2019) Thermal biology of a strictly subterranean mammalian family, the African mole-rats (Bathyergidae, Rodentia)—a review. J Therm Biol 79:166-189.

68.

Šumbera

Chitaukali

Elichová

Kubová

Burda

(2004) Microclimatic stability in burrows of an Afrotropical solitary bathyergid rodent, the silvery mole-rat (Heliophobius argenteocinereus). J Zool 263:409-416.

69.

van Jaarsveld

Bennett

Hart

Oosthuizen

(2019) Locomotor activity and body temperature rhythms in the Mahali mole-rat (C. h. mahali): the effect of light and ambient temperature variations. J Therm Biol 79:24-32.

70.

Vasicek

Oosthuizen

Cooper

Bennett

(2005) Circadian rhythms of locomotor activity in the subterranean Mashona mole rat, Cryptomys darlingi. Physiol Behav 84:181-191.

71.

Vaze

Sharma

(2013) On the adaptive significance of circadian clocks for their owners. Chronobiol Int 30:413-433.

72.

Vejmělka

Okrouhlík

Lövy

Šaffa

Nevo

Bennett

Šumbera

(2021) Heat dissipation in subterranean rodents: the role of body region and social organisation. Sci Rep 11:2029.

73.

Verwey

Robinson

Amir

(2013) Recording and analysis of circadian rhythms in running-wheel activity in rodents. Journal Vis Exp 24:e50186.

74.

Vleck

(1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Zool 52:122-136.

75.

Wallace

KME

van Jaarsveld

Bennett

Hart

(2021) The joint effect of micro- and macro-climate on the thermoregulation and heat dissipation of two African mole-rat (Bathyergidae) sub-species, Cryptomys hottentotus mahali and C. h. pretoriae. J Therm Biol 99:103025.

Ambient Temperature as a Strong Zeitgeber of Circadian Rhythms in Response to Temperature Sensitivity and Poor Heat Dissipation Abilities in Subterranean African Mole-Rats

Abstract

Keywords

Materials and Methods

Study Animals

Experimental Protocol

LA Recording

Statistical Analysis

Results

Discussion

Footnotes

Acknowledgements

Author Contributions

Conflict of Interest Statement

ORCID iDs

Data Accessibility

References